镉对长江化溪蟹心脏组织器官的毒性作用及机制研究
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摘要
本学位论文综合采用光镜、电镜、酶学检测、流式细胞术、基因克隆、实时荧光定量PCR等手段与方法,以长江华溪蟹(Sinopotamon yangtsekiense)作为研究对象,采用急性毒性实验方法,研究了不同浓度镉暴露对心脏组织器官的影响,旨在阐明镉对心脏的毒性效应和致毒机制。为了研究镉对心脏组织器官的细胞与生化毒理学效应,就心肌细胞显微与亚显微结构进行了观察,并且检测了镉的蓄积、超氧化物歧化酶(SOD)、过氧化氢酶(CAT)、谷胱甘肽过氧化物酶(GPx)三种抗氧化酶的活力和脂质过氧化产物丙二醛(MDA)的含量,探讨了心肌细胞结构改变和氧化应激之间的关系。在此基础上,为了求证镉对心脏造成氧化损伤后是否进一步诱导心肌细胞发生凋亡,分别采用Hoechst33258荧光染色法、琼脂糖凝胶电泳法、Annexin V-FITC/PI流式细胞技术和Caspase-3酶活力测定的方法,检测了镉对心肌细胞凋亡的影响。之后,为了探明心脏对镉的应答反应,采用RT-PCR技术克隆得到了长江华溪蟹一种热休克蛋白70(SyHSP70)基因的部分cDNA序列,并利用实时荧光定量PCR技术检测了镉诱导SyHSP70和MTmRNA表达的变化特征。主要研究内容和结果如下：
1、镉对长江华溪蟹主要组织器官细胞的影响
采用石蜡切片和H.E.染色方法,研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露4d后,对长江华溪蟹肝胰腺、鳃、心脏和精巢四种主要组织器官组织细胞的影响,旨在为后续研究工作奠定基础,为镉对溪蟹生化、分子水平的影响提供支持和依据。结果显示,四种组织器官均有不同程度的损伤,且随镉浓度的增大损伤不断加重。肝胰腺组织细胞的变化包括：R细胞数目持续增加、空泡化,坏死细胞脱落和腺管坏死等。鳃组织细胞：鳃叶间隙紊乱,pillar细胞系统被破坏,肾原细胞和血细胞数目增加,鳃叶变宽,多处鳃叶上皮断裂以及有毛细管扩张现象。心脏组织细胞：灶性区域变性和坏死,并伴随有炎细胞浸润现象。精巢组织细胞：生精细胞排列不规则,空泡样结构增多,初级精母细胞和次级精母细胞核固缩现象加剧,管腔内精细胞减少,生精细胞以及生精小管坏死。实验结果提示镉暴露后溪蟹主要组织器官结构的改变很可能影响了生物体的主要生理功能,例如肝胰腺的吸收、储存和分泌,鳃的呼吸、渗透和离子调节及精子发生。研究结果表明组织病理学的变化能够灵敏反映镉对甲克动物的胁迫程度及毒性大小,可作为水生态环境镉污染程度的生物评估指标。
2、镉诱导长江华溪蟹心脏组织细胞结构的改变与氧化损伤作用
采用急性体外镉暴露法,研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露1d、3d、5d、7d后长江华溪蟹心脏中镉蓄积情况和显微结构与亚显微结构、抗氧化酶活性和脂质过氧化的变化。结果显示,镉的积累具有浓度-效应关系,在镉浓度116.00mg·L-1暴露5d时积累量达到最大(14.0±1.67μg·g-1),是对照组的13.2倍。光镜观察发现,镉暴露时间较短时对心脏组织细胞的影响不明显。但是随浓度和时间的增加,出现心肌水肿、空泡变性、玻璃样变性、炎细胞浸润等病理现象。透射电镜观察显示,心肌细胞核变形、染色质浓缩边集、核固缩、核碎裂,线粒体空泡化、嵴断裂、嵴溶解,内质网膨胀,肌原纤维水肿以及有炎细胞浸润现象。心脏抗氧化酶活性也发生了不同程度的改变,SOD活性在整个处理期间显著增高,CAT和GPx活性分别在暴露5d的14.50mg·L-1和7.25mg·L-1浓度组升高,之后活性降低。MDA含量在5d和7d时显著增加,脂质过氧化加剧。结论：镉的高浓度及长时间积累对心脏有明显的毒性作用,其作用机制与氧化胁迫和脂质过氧化有关。
3、镉诱导长江华溪蟹心肌细胞凋亡的研究
采用Hoechst33258荧光染色法、琼脂糖凝胶电泳法、Annexin V-FITC/PI流式细胞术、Caspase-3酶活力测定的方法,分别从细胞形态学和生物化学水平观察和检测了急性镉暴露(7.25、14.50、29.00、58.00、116.00mg·L-1)1d、3d、5d和7d诱导长江华溪蟹心肌细胞凋亡的情况。结果显示,荧光显微镜未观察到典型的凋亡细胞核形态学变化；琼脂糖凝胶电泳图谱未出现凋亡细胞所特有的梯状条带；流式细胞技术检测发现虽然细胞凋亡率增加,但与对照组相比无统计学意义(P>0.05)；Caspase-3活性也没有显著性变化(P>0.05)。因此,在本实验所选取的浓度和时间范围内,镉未诱导长江华溪蟹心肌细胞发生细胞凋亡,这与本课题组前期研究中观察到的肝胰腺、精巢组织在染毒2d、7d发生细胞凋亡的情况明显不同。原因可能与心脏组织的特殊功能有关。
4、镉诱导长江华溪蟹心脏热休克蛋白70和金属硫蛋白基因表达的研究
采用RT-PCR技术从长江华溪蟹心脏组织中克隆得到一种热休克蛋白70(SyHSP70)基因的部分cDNA序列,长度为1735bp。将获得的cDNA序列以及推导的氨基酸序列采用BLAST程序与GenBank数据库进行同源性搜索,结果发现,该cDNA序列和氨基酸序列与甲壳动物的HSP70有极高的同源性,分别高达89%和97%。利用实时荧光定量PCR技术研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露1d、3d、5d、7d对心脏SyHSP70和MTmRNA表达的影响。结果表明,在镉浓度58.00mg·L-1、116.00mg·L-1处理1d和镉浓度7.25mg·L-1、14.50mg·L-1处理3d时SyHSP70mRNA的表达量(以(3-actin mRNA水平为内参)显著下降,但是,5d和7d的所有浓度组SyHSP70mRNA的表达无明显变化(P>0.05)。镉暴露显著诱导了心脏MT mRNA的表达,且随镉浓度的增大和暴露时间的延长,MT mRNA的表达一直增加,浓度-效应和时间-效应关系明显。本研究结果显示长江华溪蟹心脏对镉的应激机制包括MT mRNA的增加。
The freshwater crab Sinopotamon yangtsekiense (Bott,1967) is a common endemic species in China. In the preset study, S. yangtsekiense were selected as experiment animals and exposed in the laboratory to a wide range of sublethal concentrations of cadmium (Cd)(7.25,14.50,29.00,58.00,116.00mg·L-1), the histopathological alternations of hepatopancreas, gills, heart and testis were investigated. To explore the toxic effects and stress responses of Cd exposure on heart of S. yangtsekiense, we next detected the accumulation of Cd in the heart and the effects of Cd on the histopathology, antioxidant enzymes and lipid peroxidation. Then, to verify if apoptosis is one of the cardiomyocyte death pathways upon Cd administration, the effects of Cd on cardiomyocyte apoptosis in S. yangtsekiense were assayed. The present study applied morphological, biochemical, cellular, molecular and toxicological methods and technology comprehensively. The aim of this work was to clarify the mechanism of toxic effects of Cd on the heart of S. yangtsekiense and provide useful references on the healthy aquaculture and the effective evaluation of Cd pollution. The present study will enrich the database of Cd's cardiotoxicity in crustaceans. The main results and conclusions in this thesis are summarized as follows:
1. Effects of cadmium on hepatopancreas, gills, heart and testis in the freshwater crab Sinopotamon yangtsekiense
The freshwater crab S. yangtsekiense was exposed in the laboratory to a wide range of sublethal concentrations of cadmium (Cd)(7.25,14.50,29.00,58.00,116.00mg·L-1) for4days to explore the acute toxic effects. The results showed Cd caused progressive histopathological damages to the principal tissues, including hepatopancreas, gills, heart and testis. Hepatopancreas alterations included increases in the number of R-cells, extensive vacuolation, detachment of necrotic cells from basal laminae and then tubular necrosis lesion. The gills showed disordered interlamellar spaces, breakdown of pillar cell system, an increased number of nephrocytes and haemocytes, increased lamellae width, ruption of lamella epithelium as well as telangiectasia. The main histopathological alternations in the heart were characterized by degeneration and/or necrosis of focal areas accompanied with infiltration of inflammatory cells. In the testis, vacuolar degeneration, nuclear condensation, a reduction in the number of sperms lined with degeneration and/or necrosis of spermatogenic cells, atrophied seminiferous epithelia as well as tubular necrosis were noticed. These findings provide baseline information on the deleterious effects of Cd on S. yangtsekiense and suggest structural alternations of vital tissues following elevated Cd exposure, which could affect vital physiological functions, such as absorption, storage and secretion of the hepatopancreas, respiration, osmotic and ionic regulations of the gills, as well as spermatogenesis of testis. Such alternations could eventually affect the survival and reproduction of S. yangtsekiense. Thus, all possible remedial measures should be adopted to prevent Cd contamination in aquatic environments.
2. Morphologic changes and oxidative damage of the heart induced by cadmium exposure in the freshwater crab Sinopotamon yangtsekiense
Cadmium (Cd) is a highly toxic element in water. Its toxicity has been attributed to oxidative stress mediated by free radicals. Here we investigated the effects of Cd on histopathology, antioxidant enzymes and lipid peroxidation of crustacean heart. The freshwater crabs S. yangtsekiense were exposed to different concentrations of Cd for1,3,5and7days. After exposure, histological abnormalities were discovered, including myocardial edema, vacuolar and vitreous degeneration, and infiltration of inflammatory cells. Additionally, alterations in nuclei, mitochondria, rough endoplasmic reticulum as well as myofibrils were observed. Meanwhile, superoxide dismutase (SOD) activity was significantly increased after Cd exposure. Catalase (CAT) activity was only increased in the group exposed to14.50mg·L-1Cd on day5and decreased with increasing Cd concentration and exposure time. Glutathione peroxidase (GPx) activity was increased in groups treated with29.00,58.00and116.00mg·L-1on days1and3, and decreased thereafter. Besides, malondialdehyde (MDA) levels were significantly increased after3days of Cd exposure at all the indicated concentrations. These results showed that acute Cd exposure led to harmful effects on the histology of crab heart, which are most likely linked to Cd-induced oxidative stress.
3. Effects of cadmium on apoptosis of cardiomyocyte in the freshwater crab Sinopotamon yangtsekiense
The effects of cadmium (Cd) on cardiomyocyte apoptosis in the freshwater crab S. yangtsekiense were investigated by acute systemic toxicity testing methods. To verify if apoptosis is one of the cardiomyocyte death pathways upon Cd administration, crabs were exposed to different concentrations of Cd (7.25,14.50,29.00,58.00and116.00mg·L-1) for1,3,5and7days. The results showed the characteristic apoptotic morphologic changes and “ladder” pattern were not observed by fluorescence microscopy with Hoechst33258staining and agarose gel electrophoresis. Flow cytometry assay indicated that the percentage of apoptotic cells was increased with the increasing of exposure time and concentrations of Cd compared with control, but there was no significant difference. Moreover, the activity of Caspase-3was not affected by Cd treatment after7days of exposure. However, these findings suggest that apoptosis was not induced by Cd in cardiomyocytes according to the result of the present study. While previous studies in our lab showed that Cd induced apoptosis in the hepatopancreas and testis cells of crabs after2days and7days of exposure. In the crab cardiomyocyte, the lack of Cd-induced apoptosis may be attributed to different Cd accumulation levels in the three tissues.
4. Expression analysis of heat shock protein70and metallothionein genes in heart of the freshwater crab Sinopotamon yangtsekiense in response to cadmium
In order to elucidate the molecular mechanisms of the freshwater crab S. yangtsekiense response to cadmium (Cd) stress, we cloned and sequenced a partial cDNA encoding a70kDa heat shock protein (SyHSP70) from the heart of S. yangtsekiense. Next we investigated its time-and dose-related effects by quantitative real-time PCR on mRNA levels of SyHSP70and metallothionein (MT) in the heart of crabs. The results showed the expression of SyHSP70mRNA decreased significantly after exposure to58.00mg·L-1,116.00mg·L-1Cd for1day or7.25mg·L-1,14.50mg·L-1for3days. While the expression of MT mRNA increased significantly with increasing Cd concentration and exposure time. These results indicate that MT plays an important role in the physiological changes related to metabolism and cell protection that occur in S. yangtsekiense exposed to Cd. This is the first report on the expression of HSP70induced by Cd in S. yangtsekiense.
1、镉对长江华溪蟹主要组织器官细胞的影响
采用石蜡切片和H.E.染色方法,研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露4d后,对长江华溪蟹肝胰腺、鳃、心脏和精巢四种主要组织器官组织细胞的影响,旨在为后续研究工作奠定基础,为镉对溪蟹生化、分子水平的影响提供支持和依据。结果显示,四种组织器官均有不同程度的损伤,且随镉浓度的增大损伤不断加重。肝胰腺组织细胞的变化包括：R细胞数目持续增加、空泡化,坏死细胞脱落和腺管坏死等。鳃组织细胞：鳃叶间隙紊乱,pillar细胞系统被破坏,肾原细胞和血细胞数目增加,鳃叶变宽,多处鳃叶上皮断裂以及有毛细管扩张现象。心脏组织细胞：灶性区域变性和坏死,并伴随有炎细胞浸润现象。精巢组织细胞：生精细胞排列不规则,空泡样结构增多,初级精母细胞和次级精母细胞核固缩现象加剧,管腔内精细胞减少,生精细胞以及生精小管坏死。实验结果提示镉暴露后溪蟹主要组织器官结构的改变很可能影响了生物体的主要生理功能,例如肝胰腺的吸收、储存和分泌,鳃的呼吸、渗透和离子调节及精子发生。研究结果表明组织病理学的变化能够灵敏反映镉对甲克动物的胁迫程度及毒性大小,可作为水生态环境镉污染程度的生物评估指标。
2、镉诱导长江华溪蟹心脏组织细胞结构的改变与氧化损伤作用
采用急性体外镉暴露法,研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露1d、3d、5d、7d后长江华溪蟹心脏中镉蓄积情况和显微结构与亚显微结构、抗氧化酶活性和脂质过氧化的变化。结果显示,镉的积累具有浓度-效应关系,在镉浓度116.00mg·L-1暴露5d时积累量达到最大(14.0±1.67μg·g-1),是对照组的13.2倍。光镜观察发现,镉暴露时间较短时对心脏组织细胞的影响不明显。但是随浓度和时间的增加,出现心肌水肿、空泡变性、玻璃样变性、炎细胞浸润等病理现象。透射电镜观察显示,心肌细胞核变形、染色质浓缩边集、核固缩、核碎裂,线粒体空泡化、嵴断裂、嵴溶解,内质网膨胀,肌原纤维水肿以及有炎细胞浸润现象。心脏抗氧化酶活性也发生了不同程度的改变,SOD活性在整个处理期间显著增高,CAT和GPx活性分别在暴露5d的14.50mg·L-1和7.25mg·L-1浓度组升高,之后活性降低。MDA含量在5d和7d时显著增加,脂质过氧化加剧。结论：镉的高浓度及长时间积累对心脏有明显的毒性作用,其作用机制与氧化胁迫和脂质过氧化有关。
3、镉诱导长江华溪蟹心肌细胞凋亡的研究
采用Hoechst33258荧光染色法、琼脂糖凝胶电泳法、Annexin V-FITC/PI流式细胞术、Caspase-3酶活力测定的方法,分别从细胞形态学和生物化学水平观察和检测了急性镉暴露(7.25、14.50、29.00、58.00、116.00mg·L-1)1d、3d、5d和7d诱导长江华溪蟹心肌细胞凋亡的情况。结果显示,荧光显微镜未观察到典型的凋亡细胞核形态学变化；琼脂糖凝胶电泳图谱未出现凋亡细胞所特有的梯状条带；流式细胞技术检测发现虽然细胞凋亡率增加,但与对照组相比无统计学意义(P>0.05)；Caspase-3活性也没有显著性变化(P>0.05)。因此,在本实验所选取的浓度和时间范围内,镉未诱导长江华溪蟹心肌细胞发生细胞凋亡,这与本课题组前期研究中观察到的肝胰腺、精巢组织在染毒2d、7d发生细胞凋亡的情况明显不同。原因可能与心脏组织的特殊功能有关。
4、镉诱导长江华溪蟹心脏热休克蛋白70和金属硫蛋白基因表达的研究
采用RT-PCR技术从长江华溪蟹心脏组织中克隆得到一种热休克蛋白70(SyHSP70)基因的部分cDNA序列,长度为1735bp。将获得的cDNA序列以及推导的氨基酸序列采用BLAST程序与GenBank数据库进行同源性搜索,结果发现,该cDNA序列和氨基酸序列与甲壳动物的HSP70有极高的同源性,分别高达89%和97%。利用实时荧光定量PCR技术研究了7.25、14.50、29.00、58.00、116.00mg·L-1镉暴露1d、3d、5d、7d对心脏SyHSP70和MTmRNA表达的影响。结果表明,在镉浓度58.00mg·L-1、116.00mg·L-1处理1d和镉浓度7.25mg·L-1、14.50mg·L-1处理3d时SyHSP70mRNA的表达量(以(3-actin mRNA水平为内参)显著下降,但是,5d和7d的所有浓度组SyHSP70mRNA的表达无明显变化(P>0.05)。镉暴露显著诱导了心脏MT mRNA的表达,且随镉浓度的增大和暴露时间的延长,MT mRNA的表达一直增加,浓度-效应和时间-效应关系明显。本研究结果显示长江华溪蟹心脏对镉的应激机制包括MT mRNA的增加。
The freshwater crab Sinopotamon yangtsekiense (Bott,1967) is a common endemic species in China. In the preset study, S. yangtsekiense were selected as experiment animals and exposed in the laboratory to a wide range of sublethal concentrations of cadmium (Cd)(7.25,14.50,29.00,58.00,116.00mg·L-1), the histopathological alternations of hepatopancreas, gills, heart and testis were investigated. To explore the toxic effects and stress responses of Cd exposure on heart of S. yangtsekiense, we next detected the accumulation of Cd in the heart and the effects of Cd on the histopathology, antioxidant enzymes and lipid peroxidation. Then, to verify if apoptosis is one of the cardiomyocyte death pathways upon Cd administration, the effects of Cd on cardiomyocyte apoptosis in S. yangtsekiense were assayed. The present study applied morphological, biochemical, cellular, molecular and toxicological methods and technology comprehensively. The aim of this work was to clarify the mechanism of toxic effects of Cd on the heart of S. yangtsekiense and provide useful references on the healthy aquaculture and the effective evaluation of Cd pollution. The present study will enrich the database of Cd's cardiotoxicity in crustaceans. The main results and conclusions in this thesis are summarized as follows:
1. Effects of cadmium on hepatopancreas, gills, heart and testis in the freshwater crab Sinopotamon yangtsekiense
The freshwater crab S. yangtsekiense was exposed in the laboratory to a wide range of sublethal concentrations of cadmium (Cd)(7.25,14.50,29.00,58.00,116.00mg·L-1) for4days to explore the acute toxic effects. The results showed Cd caused progressive histopathological damages to the principal tissues, including hepatopancreas, gills, heart and testis. Hepatopancreas alterations included increases in the number of R-cells, extensive vacuolation, detachment of necrotic cells from basal laminae and then tubular necrosis lesion. The gills showed disordered interlamellar spaces, breakdown of pillar cell system, an increased number of nephrocytes and haemocytes, increased lamellae width, ruption of lamella epithelium as well as telangiectasia. The main histopathological alternations in the heart were characterized by degeneration and/or necrosis of focal areas accompanied with infiltration of inflammatory cells. In the testis, vacuolar degeneration, nuclear condensation, a reduction in the number of sperms lined with degeneration and/or necrosis of spermatogenic cells, atrophied seminiferous epithelia as well as tubular necrosis were noticed. These findings provide baseline information on the deleterious effects of Cd on S. yangtsekiense and suggest structural alternations of vital tissues following elevated Cd exposure, which could affect vital physiological functions, such as absorption, storage and secretion of the hepatopancreas, respiration, osmotic and ionic regulations of the gills, as well as spermatogenesis of testis. Such alternations could eventually affect the survival and reproduction of S. yangtsekiense. Thus, all possible remedial measures should be adopted to prevent Cd contamination in aquatic environments.
2. Morphologic changes and oxidative damage of the heart induced by cadmium exposure in the freshwater crab Sinopotamon yangtsekiense
Cadmium (Cd) is a highly toxic element in water. Its toxicity has been attributed to oxidative stress mediated by free radicals. Here we investigated the effects of Cd on histopathology, antioxidant enzymes and lipid peroxidation of crustacean heart. The freshwater crabs S. yangtsekiense were exposed to different concentrations of Cd for1,3,5and7days. After exposure, histological abnormalities were discovered, including myocardial edema, vacuolar and vitreous degeneration, and infiltration of inflammatory cells. Additionally, alterations in nuclei, mitochondria, rough endoplasmic reticulum as well as myofibrils were observed. Meanwhile, superoxide dismutase (SOD) activity was significantly increased after Cd exposure. Catalase (CAT) activity was only increased in the group exposed to14.50mg·L-1Cd on day5and decreased with increasing Cd concentration and exposure time. Glutathione peroxidase (GPx) activity was increased in groups treated with29.00,58.00and116.00mg·L-1on days1and3, and decreased thereafter. Besides, malondialdehyde (MDA) levels were significantly increased after3days of Cd exposure at all the indicated concentrations. These results showed that acute Cd exposure led to harmful effects on the histology of crab heart, which are most likely linked to Cd-induced oxidative stress.
3. Effects of cadmium on apoptosis of cardiomyocyte in the freshwater crab Sinopotamon yangtsekiense
The effects of cadmium (Cd) on cardiomyocyte apoptosis in the freshwater crab S. yangtsekiense were investigated by acute systemic toxicity testing methods. To verify if apoptosis is one of the cardiomyocyte death pathways upon Cd administration, crabs were exposed to different concentrations of Cd (7.25,14.50,29.00,58.00and116.00mg·L-1) for1,3,5and7days. The results showed the characteristic apoptotic morphologic changes and “ladder” pattern were not observed by fluorescence microscopy with Hoechst33258staining and agarose gel electrophoresis. Flow cytometry assay indicated that the percentage of apoptotic cells was increased with the increasing of exposure time and concentrations of Cd compared with control, but there was no significant difference. Moreover, the activity of Caspase-3was not affected by Cd treatment after7days of exposure. However, these findings suggest that apoptosis was not induced by Cd in cardiomyocytes according to the result of the present study. While previous studies in our lab showed that Cd induced apoptosis in the hepatopancreas and testis cells of crabs after2days and7days of exposure. In the crab cardiomyocyte, the lack of Cd-induced apoptosis may be attributed to different Cd accumulation levels in the three tissues.
4. Expression analysis of heat shock protein70and metallothionein genes in heart of the freshwater crab Sinopotamon yangtsekiense in response to cadmium
In order to elucidate the molecular mechanisms of the freshwater crab S. yangtsekiense response to cadmium (Cd) stress, we cloned and sequenced a partial cDNA encoding a70kDa heat shock protein (SyHSP70) from the heart of S. yangtsekiense. Next we investigated its time-and dose-related effects by quantitative real-time PCR on mRNA levels of SyHSP70and metallothionein (MT) in the heart of crabs. The results showed the expression of SyHSP70mRNA decreased significantly after exposure to58.00mg·L-1,116.00mg·L-1Cd for1day or7.25mg·L-1,14.50mg·L-1for3days. While the expression of MT mRNA increased significantly with increasing Cd concentration and exposure time. These results indicate that MT plays an important role in the physiological changes related to metabolism and cell protection that occur in S. yangtsekiense exposed to Cd. This is the first report on the expression of HSP70induced by Cd in S. yangtsekiense.
引文
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